Identification of the Candida albicans Cap1p regulon

Eukaryotic Cell

Volumn 8, Issue 6, 2009, Pages 806-820

  Znaidi, Sadri ^a   Barker, Katherine S ^b,c   Weber, Sandra ^a   Alarco, Anne Marie ^a,e   Liu, Teresa T ^b,c   Boucher, Geneviève ^a   Rogers, P David ^b,c   Raymond, Martine ^a,d  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c LE BONHEUR CHILDREN'S MEDICAL CENTER   (United States)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

^e Genome Quebec   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CAP1 PROTEIN, CANDIDA ALBICANS; CELL CYCLE PROTEIN; FUNGAL PROTEIN; TRANSACTIVATOR PROTEIN;

ARTICLE; BINDING SITE; CANDIDA ALBICANS; CHEMISTRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; REGULON;

BINDING SITES; CANDIDA ALBICANS; CELL CYCLE PROTEINS; CONSERVED SEQUENCE; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; PROTEIN BINDING; REGULON; TRANS-ACTIVATORS;

CANDIDA ALBICANS;

EID: 66749094808     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00002-09     Document Type: Article

References (71)

1. Akins, R. A. 2005. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43:285-318.
2. Alarco, A.-M., I. Balan, D. Talibi, N. Mainville, and M. Raymond. 1997. AP1-mediated multidrug resistance in Saccharomyces cerevisiae requires FLR1 encoding a transporter of the major facilitator superfamily. J. Biol. Chem. 272:19304-19313.
3. Alarco, A.-M., and M. Raymond. 1999. The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans. J. Bacteriol. 181:700-708 (Pubitemid 29061549).
4. Alonso-Monge, R., F. Navarro-Garcia, E. Roman, A. I. Negredo, B. Eisman, C. Nombela, and J. Pla. 2003. The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot. Cell 2:351-361 (Pubitemid 36562374).
5. Balakrishnan, S. K., and D. S. Gross. 2008. The tumor suppressor p53 associates with gene coding regions and co-traverses with elongating RNA polymerase II in an in vivo model. Oncogene 27:2661-2672.
6. Buck, M. J., and J. D. Lieb. 2004. ChIP-chip: considerations for the design, analysis, and application of genome-wide chromatin immunoprecipitation experiments. Genomics 83:349-360 (Pubitemid 38220840).
7. Bustamante, C. I. 2005. Treatment of Candida infection: a view from the trenches! Curr. Opin. Infect. Dis. 18:490-495.
8. Calabrese, D., J. Bille, and D. Sanglard. 2000. A novel multidrug efflux transporter gene of the major facilitator superfamily from Candida albicans (FLU1) conferring resistance to fluconazole. Microbiology 146:2743-2754.
9. Care, R. S., J. Trevethick, K. M. Binley, and P. E. Sudbery. 1999. The MET3 promoter: a new tool for Candida albicans molecular genetics. Mol. Microbiol. 34:792-798.
10. Carlson, J. M., A. Chakravarty, C. E. DeZiel, and R. H. Gross. 2007. SCOPE: a web server for practical de novo motif discovery. Nucleic Acids Res. 35:W259-W264.
11. Carroll, J. S., C. A. Meyer, J. Song, W. Li, T. R. Geistlinger, J. Eeckhoute, A. S. Brodsky, E. K. Keeton, K. C. Fertuck, G. F. Hall, Q. Wang, S. Bekiranov, V. Sementchenko, E. A. Fox, P. A. Silver, T. R. Gingeras, X. S. Liu, and M. Brown. 2006. Genome-wide analysis of estrogen receptor binding sites. Nat. Genet. 38:1289-1297.
12. Chakravarty, A., J. M. Carlson, R. S. Khetani, and R. H. Gross. 2007. A novel ensemble learning method for de novo computational identification of DNA binding sites. BMC Bioinform. 8:249 (Pubitemid 47287982).
13. Chauhan, N., J. P. Latge, and R. Calderone. 2006. Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus. Nat. Rev. Microbiol. 4:435-444.
14. Chua, G., Q. D. Morris, R. Sopko, M. D. Robinson, O. Ryan, E. T. Chan, B. J. Frey, B. J. Andrews, C. Boone, and T. R. Hughes. 2006. Identifying transcription factor functions and targets by phenotypic activation. Proc. Natl. Acad. Sci. USA 103:12045-12050.
15. Coste, A., A. Selmecki, A. Forche, D. Diogo, M. E. Bougnoux, C. d'Enfert, J. Berman, and D. Sanglard. 2007. Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot. Cell 6:18891904.
16. Coste, A., V. Turner, F. Ischer, J. Morschhauser, A. Forche, A. Selmecki, J. Berman, J. Bille, and D. Sanglard. 2006. A mutation in Tac1p, a transcription factor regulating CDR1 and CDR2, is coupled with loss of heterozygosity at chromosome 5 to mediate antifungal resistance in Candida albicans. Genetics 172:2139-2156.
17. Coste, A. T., M. Karababa, F. Ischer, J. Bille, and D. Sanglard. 2004. TAC1, transcriptional activator of CDR genes, is a new transcription factor involved in the regulation of Candida albicans ABC transporters CDR1 and CDR2. Eukaryot. Cell 3:1639-1652 (Pubitemid 40025121).
18. de Repentigny, L., D. Lewandowski, and P. Jolicoeur. 2004. Immunopathogenesis of oropharyngeal candidiasis in human immunodeficiency virus infection. Clin. Microbiol. Rev. 17:729-759.
19. Dunkel, N., J. Blass, P. D. Rogers, and J. Morschhauser. 2008. Mutations in the multi-drug resistance regulator MRR1, followed by loss of heterozygosity, are the main cause of MDR1 overexpression in fluconazole-resistant Candida albicans strains. Mol. Microbiol. 69:827-840.
20. Dunkel, N., T. T. Liu, K. S. Barker, R. Homayouni, J. Morschhauser, and P. D. Rogers. 2008. A gain-of-function mutation in the transcription factor Upc2p causes upregulation of ergosterol biosynthesis genes and increased fluconazole resistance in a clinical Candida albicans isolate. Eukaryot. Cell 7:1180-1190.
21. Eggimann, P., J. Garbino, and D. Pittet. 2003. Management of Candida species infections in critically ill patients. Lancet Infect. Dis. 3:772-785.
22. Enjalbert, B., D. A. Smith, M. J. Cornell, I. Alam, S. Nicholls, A. J. Brown, and J. Quinn. 2006. Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol. Biol. Cell 17:1018-1032 (Pubitemid 43191132).
23. Fonzi, W. A., and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
24. Fradin, C, P. De Groot, D. MacCallum, M. Schaller, F. Klis, F. C. Odds, and B. Hube. 2005. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 56:397-415.
25. Goldman, G. H., M. E. Silva Ferreira, M. E. dos Reis, M. Savoldi, D. Perlin, S. Park, P. C. Godoy Martinez, M. H. Goldman, and A. L. Colombo. 2004. Evaluation of fluconazole resistance mechanisms in Candida albicans clinical isolates from HIV-infected patients in Brazil. Diagn. Microbiol. Infect. Dis. 50:25-32.
26. Harry, J. B., B. G. Oliver, J. L. Song, P. M. Silver, J. T. Little, J. Choiniere, and T. C. White. 2005. Drug-induced regulation of the MDR1 promoter in Candida albicans. Antimicrob. Agents Chemother. 49:2785-2792.
27. Herrero, E., J. Ros, G. Belli, and E. Cabiscol. 2008. Redox control and oxidative stress in yeast cells. Biochim. Biophys. Acta 1780:1217-1235.
28. Hiller, D., S. Stahl, and J. Morschhauser. 2006. Multiple cis-acting sequences mediate upregulation of the MDR1 efflux pump in a fluconazoleresistant clinical Candida albicans isolate. Antimicrob. Agents Chemother. 50:2300-2308 (Pubitemid 43993166).
29. Jia, X. M., Z. P. Ma, Y. Jia, P. H. Gao, J. D. Zhang, Y. Wang, Y. G. Xu, L. Wang, Y. Y. Cao, Y. B. Cao, L. X. Zhang, and Y. Y. Jiang. 2008. RTA2, a novel gene involved in azole resistance in Candida albicans. Biochem. Biophys. Res. Commun. 373:631-636.
30. Karababa, M., A. T. Coste, B. Rognon, J. Bille, and D. Sanglard. 2004. Comparison of gene expression profiles of Candida albicans azole-resistant clinical isolates and laboratory strains exposed to drugs inducing multidrug transporters. Antimicrob. Agents Chemother. 48:3064-3079.
31. Kelly, R., S. M. Miller, M. B. Kurtz, and D. R. Kirsch. 1987. Directed mutagenesis in Candida albicans: one-step gene disruption to isolate ura3 mutants. Mol. Cell. Biol. 7:199-208 (Pubitemid 17230400).
32. Kraemer, S. M., D. A. Goldstrohm, A. Berger, S. Hankey, S. A. Rovinsky, W. Scott Moye-Rowley, and L. A. Stargell. 2006. TFIIA plays a role in the response to oxidative stress. Eukaryot. Cell 5:1081-1090 (Pubitemid 44100706).
33. Kuge, S., M. Arita, A. Murayama, K. Maeta, S. Izawa, Y. Inoue, and A. Nomoto. 2001. Regulation of the yeast Yap1p nuclear export signal is mediated by redox signal-induced reversible disulfide bond formation. Mol. Cell. Biol. 21:6139-6150.
34. Kuge, S., N. Jones, and A. Nomoto. 1997. Regulation of yAP-1 nuclear localization in response to oxidative stress. EMBO J. 16:1710-1720 (Pubitemid 27151965).
35. Kuge, S., T. Toda, N. Iizuka, and A. Nomoto. 1998. Crm1 (XpoI) dependent nuclear export of the budding yeast transcription factor yAP-1 is sensitive to oxidative stress. Genes Cells 3:521-532 (Pubitemid 28475322).
36. Kusch, H., S. Engelmann, D. Albrecht, J. Morschhauser, and M. Hecker. 2007. Proteomic analysis of the oxidative stress response in Candida albicans. Proteomics 7:686-697.
37. Lavoie, H., A. Sellam, C. Askew, A. Nantel, and M. Whiteway. 2008. A toolbox for epitope-tagging and genome-wide location analysis in Candida albicans. BMC Genomics 9:578.
38. Liu, T. T., S. Znaidi, K. S. Barker, L. Xu, R. Homayouni, S. Saidane, J. Morschhauser, A. Nantel, M. Raymond, and P. D. Rogers. 2007. Genomewide expression and location analyses of the Candida albicans Tac1p regulon. Eukaryot. Cell 6:2122-2138.
39. Lucau-Danila, A., G. Lelandais, Z. Kozovska, V. Tanty, T. Delaveau, F. Devaux, and C. Jacq. 2005. Early expression of yeast genes affected by chemical stress. Mol. Cell. Biol. 25:1860-1868.
40. Lupetti, A., R. Danesi, M. Campa, M. Del Tacca, and S. Kelly. 2002. Molecular basis of resistance to azole antifungals. Trends Mol. Med. 8:76-81.
41. MacPherson, S., B. Akache, S. Weber, X. De Deken, M. Raymond, and B. Turcotte. 2005. Candida albicans zinc cluster protein Upc2p confers resistance to antifungal drugs and is an activator of ergosterol biosynthetic genes. Antimicrob. Agents Chemother. 49:1745-1752.
42. MacPherson, S., M. Larochelle, and B. Turcotte. 2006. A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol. Mol. Biol. Rev. 70:583-604.
43. Maeta, K., S. Izawa, S. Okazaki, S. Kuge, and Y. Inoue. 2004. Activity of the Yap1 transcription factor in Saccharomyces cerevisiae is modulated by methylglyoxal, a metabolite derived from glycolysis. Mol. Cell. Biol. 24:8753-8764.
44. McCarroll, N. E., A. Protzel, Y. Ioannou, H. F. Frank Stack, M. A. Jackson, M. D. Waters, and K. L. Dearfield. 2002. A survey of EPA/OPP and open literature on selected pesticide chemicals. III. Mutagenicity and carcinogenicity of benomyl and carbendazim. Mutat. Res. 512:1-35.
45. Molin, M., J. P. Renault, G. Lagniel, S. Pin, M. Toledano, and J. Labarre. 2007. Ionizing radiation induces a Yapl-dependent peroxide stress response in yeast. Free Radic. Biol. Med. 43:136-144.
46. Morschhäuser, J. 2002. The genetic basis of fluconazole resistance development in Candida albicans. Biochim. Biophys. Acta 1587:240-248.
47. Morschhäuser, J., K. S. Barker, T. T. Liu, J. Blass-Warmuth, R. Homayouni, and P. D. Rogers. 2007. The transcription factor Mrr1p controls expression of the MDR1 efflux pump and mediates multidrug resistance in Candida albicans. PLoS Pathog. 3:el64 (Pubitemid 350291598).
48. Moye-Rowley, W. S. 2003. Regulation of the transcriptional response to oxidative stress in fungi: similarities and differences. Eukaryot. Cell 2:381389.
49. Nguyên, D. T., A. M. Alarco, and M. Raymond. 2001. Multiple Yap1pbinding sites mediate induction of the yeast major facilitator FLR1 gene in response to drugs, oxidants, and alkylating agents. J. Biol. Chem. 276:11381145.
50. Pappas, P. G., J. H. Rex, J. D. Sobel, S. G. Filler, W. E. Dismukes, T. J. Walsh, and J. E. Edwards. 2004. Guidelines for treatment of candidiasis. Clin. Infect. Dis. 38:161-189.
51. Peng, S., A. A. Alekseyenko, E. Larschan, M. I. Kuroda, and P. J. Park. 2007. Normalization and experimental design for ChIP-chip data. BMC Bioinform. 8:219 (Pubitemid 47040417).
52. Riggle, P. J., and C. A. Kumamoto. 2006. Transcriptional regulation of MDR1, encoding a drug efflux determinant, in fluconazole-resistant Candida albicans strains through an Mcm1p binding site. Eukaryot. Cell 5:1957-1968.
53. Rognon, B., Z. Kozovska, A. T. Coste, G. Pardini, and D. Sanglard. 2006. Identification of promoter elements responsible for the regulation of MDR1 from Candida albicans, a major facilitator transporter involved in azole resistance. Microbiology 152:3701-3722.
54. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
55. Saidane, S., S. Weber, X. De Deken, G. St-Germain, and M. Raymond. 2006. PDR16-mediated azole resistance in Candida albicans. Mol. Microbiol. 60: 1546-1562.
56. Sanglard, D., and F. C. Odds. 2002. Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect. Dis. 2:73-85.
57. Schmitt, M. E., T. A. Brown, and B. L. Trumpower. 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 18:3091-3092.
58. Schneider, B. L., W. Seufert, B. Steiner, Q. H. Yang, and A. B. Futcher. 1995. Use of polymerase chain reaction epitope tagging for protein tagging in Saccharomyces cerevisiae. Yeast 11:1265-1274.
59. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
60. Sopko, R., D. Huang, N. Preston, G. Chua, B. Papp, K. Kafadar, M. Snyder, S. G. Oliver, M. Cyert, T. R. Hughes, C. Boone, and B. Andrews. 2006. Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell 21:319-330 (Pubitemid 43163527).
61. Srikantha, T., A. R. Borneman, K. J. Daniels, C. Pujol, W. Wu, M. R. Seringhaus, M. Gerstein, S. Yi, M. Snyder, and D. R. Soll. 2006. TOS9 regulates white-opaque switching in Candida albicans. Eukaryot. Cell 5:1674-1687.
62. Tang, L., X. Liu, and N. D. Clarke. 2006. Inferring direct regulatory targets from expression and genome location analyses: a comparison of transcription factor deletion and overexpression. BMC Genomics 7:215 (Pubitemid 44323649).
63. Wang, Y., Y. Y. Cao, Y. B. Cao, D. J. Wang, X. M. Jia, X. P. Fu, J. D. Zhang, Z. Xu, K. Ying, W. S. Chen, and Y. Y. Jiang. 2007. Cap1p plays regulation roles in redox, energy metabolism and substance transport: an investigation on Candida albicans under normal culture condition. Front. Biosci. 12:145153.
64. Wang, Y., Y. Y. Cao, X. M. Jia, Y. B. Cao, P. H. Gao, X. P. Fu, K. Ying, W. S. Chen, and Y. Y. Jiang. 2006. Cap1p is involved in multiple pathways of oxidative stress response in Candida albicans. Free Radic. Biol. Med. 40: 1201-1209.
65. 2 and diamide. J. Biol. Chem. 272:7908-7914.
66. Wirsching, S., S. Michel, and J. Morschhauser. 2000. Targeted gene disruption in Candida albicans wild-type strains: the role of the MDR1 gene in fluconazole resistance of clinical Candida albicans isolates. Mol. Microbiol. 36:856-865 (Pubitemid 30326531).
67. Yan, C, L. H. Lee, and L. I. Davis. 1998. Crm1p mediates regulated nuclear export of a yeast AP-1-like transcription factor. EMBO J. 17:7416-7429.
68. Zhang, X., M. de Micheli, S. T. Coleman, D. Sanglard, and W. S. MoyeRowley. 2000. Analysis of the oxidative stress regulation of the Candida albicans transcription factor, Cap1p. Mol. Microbiol. 36:618-629.
69. Zhang, Z. D., J. Rozowsky, H. Y. Lam, J. Du, M. Snyder, and M. Gerstein. 2007. Tilescope: online analysis pipeline for high-density tiling microarray data. Genome Biol. 8:R81.
70. Znaidi, S., X. De Deken, S. Weber, T. Rigby, A. Nantel, and M. Raymond. 2007. The zinc cluster transcription factor Tac1p regulates PDR16 expression in Candida albicans. Mol. Microbiol. 66:440-452 (Pubitemid 47482385)
71. Znaidi, S., S. Weber, O. Z. Al Abdin, P. Bomme, S. Saidane, S. Drouin, S. Lemieux, X. De Deken, F. Robert, and M. Raymond. 2008. Genomewide location analysis of Candida albicans Upc2p, a regulator of sterol metabolism and azole drug resistance. Eukaryot. Cell 7:836-847.